Skip to main content
SpringerLink
Log in

Opsin-immunoreactive outer segments in the pineal and parapineal organs of the lamprey (Lampetra fluviatilis), the eel (Anguilla anguilla), and the rainbow trout (Salmo gairdneri)

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The pineal complex of Lampetra fluviatilis, Anguilla anguilla and Salmo gairdneri was studied by means of the indirect immunohistochemical antiopsin reaction.

Opsin-immunoreactive material was demonstrated in the outer segments of the photoreceptor cells in the pineal organ of all three species investigated. In the lamprey, the opsin-positive outer segments were located in the lumen of the pineal vesicle and atrium. In the two teleost species, the immunoreactive outer segments were observed in abundance in the pineal end-vesicle and stalk. These structures were found to accumulate in the prominent initial portion of the pineal stalk of the eel. In the rainbow trout, immunoreactive outer segments occurred in the wide orifice of the pineal recess at the roof of the third ventricle.

In addition, outer segments of photoreceptor cells of the parapineal organ (“parapinealocytes”) displayed opsin immunoreactivity. In the lamprey, opsin immunoreactivity was restricted to the central portion of the ventral parapineal retina, while the parapinealocytes in the lateral portions did not bind the antibody. In the two teleosts, immunoreactive outer segments displayed a scattered pattern.

These immunocytochemical results provide direct evidence that the photosensitivity of the pineal demonstrated electrophysiologically in lampreys and teleosts (cf. Dodt 1973) is based on an opsin-containing photopigment. The presence of opsin in cells of the parapineal organ strengthens the view that also this organ may be capable of direct light perception. In the lamprey, the exclusive opsin immunoreactivity of a circumscribed group of parapineal cells suggests the existence of two types of parapinealocytes. The significance of opsin-containing photoreceptor outer segments occurring in the most proximal portion of the teleost pineal stalk is discussed, especially with regard to the interpretation of results obtained from pinealectomy experiments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ali MA, Wagner HJ (1975) Visual pigments: physiology and ecology. In: Ali MA (ed) Vision in fishes. Plenum Publ. Corp., New York, pp 481–516

    Google Scholar 

  • Bargmann W (1943) Die Epiphysis cerebri. In: Möllendorff W (ed) Handbuch der mikroskopischen Anatomie des Menschen, VI/1. Springer, Berlin pp 309–505

    Google Scholar 

  • Basinger SF, Hoffman RT (1982) Rhodopsin biosynthesis in isolated retinas: Methods in Enzymology 81:772–782

    Google Scholar 

  • Bertolini B, Manglia F (1966) Osservazioni sulla ultrastructura dell' occhio pineale della lampedra. Rend Acc Lincei 41:147–153

    Google Scholar 

  • Blaustein DI, Dewey NM (1979) Localization of rhodopsin in isolated osmotically intact rod outer segment discs. J Histochem Cytochem 27:788–793

    Google Scholar 

  • Bok D (1982) Renewal of photoreceptor cells. Methods in Enzymology 81:763–772

    Google Scholar 

  • Breucker H, Horstmann E (1965) Elektronenmikroskopische Untersuchungen am Pinealorgan der Regenbogenforelle (Salmo irideus). Progr Brain Res 10:259–269

    Google Scholar 

  • Cole WC, Youson JH (1982) Morphology of the pineal complex of the anadromous sea lamprey, Petromyzon marinus L. Am J Anat 165:131–163

    Google Scholar 

  • Collin JP (1969a) Cellules ganglionnaires et tractus de l'organe pinéal de Lampetra planeri. J Neuro-Visc Relat 31: 308–333

    Google Scholar 

  • Collin JP (1969b) Contribution à l'étude de l'organe pinéal. De l'épiphyse sensorielle à la glande pinéale: modalités de transformation et implications fonctionelles. Ann Stn Biol (Besse-en-Chandesse/France) Suppl 1:1–359

    Google Scholar 

  • Collin JP, Oksche A (1981) Structural and functional relationships in the nonmammalian pineal organ. In: Reiter RJ (ed) The pineal gland: Anatomy and Biochemistry, Vol I, CRC Press, Boca Raton, Florida, pp 27–67

    Google Scholar 

  • Converse CA, Papermaster DS (1975) Membrane protein analysis by two-dimensional immunoelectrophoresis. Science (Wash DC) 189:469–472

    Google Scholar 

  • Dartnall HJA, Lander MR, Munz FW (1961) Periodic changes in the visual pigment of a fish. Progr Photobiol, Proc 3rd Int Photobiol Congr, Elsevier, Amsterdam, pp 203–213

    Google Scholar 

  • Dodt E (1963) Photosensitivity of the pineal organ in the teleost, Salmo irideus (Gibbons). Experientia 19:642

    Google Scholar 

  • Dodt E (1973) The parietal eye (pineal and parapineal organs) of lower vertebrates. In: Jung R (ed) Handbook of physiology VII/3B, Springer, Berlin Heidelberg New York, pp 113–140

    Google Scholar 

  • Eakin R (1962) Lines of evolution of photoreceptors. J Gen Physiol 46:357 A-367 A

    Google Scholar 

  • Eddy JMP, Strahan R (1968) The role of the pineal complex in the pigmentary effector system of the lampreys, Mordacia mordax (Richardson) and Geotria australis Gray. Gen Comp Endocrinol 11:528–534

    Google Scholar 

  • Fenwick JC (1969) The pineal organ. In: Hoar WS, Randall DJ (eds) Fish physiology Vol 4, Academic Press, New York, pp 91–108

    Google Scholar 

  • Fenwick JC (1970) Effects of pinealectomy and bilateral enucleation on the phototactic response and the conditioned response to light of the goldfish, Carassius auratus. Can J Zool 48:175–182

    Google Scholar 

  • Gordon J, Shapley RM, Kaplan E (1978) The eel retina: Receptor classes and spectral mechanisms. J Gen Physiol 71:123–138

    Google Scholar 

  • Hafeez MA, Zerihun L (1974) Studies on central projections of the pineal nerve tract in rainbow trout, Salmo gairdneri Richardson, using cobalt chloride iontophoresis. Cell Tissue Res 154:485–510

    Google Scholar 

  • Hamasaki DI, Streck P (1971) Properties of the epiphysis cerebri of the small-spotted dogfish, Scyliorhinus canicula L. Vision Res 11:189–198

    Google Scholar 

  • Hanyu I, Niwa H (1970) Pineal photosensitivity in three teleosts, Salmo irideus, Plecoglossus altivelis and Mugil cephalus. Rev Can Biol 29:133–140

    Google Scholar 

  • Hanyu I, Niwa H, Tamura T (1978) Salient features of photosensory function of the teleostean pineal organ. Comp Biochem Physiol 61 A:49–54

    Google Scholar 

  • Hárosi FI (1982) Polarized microspectrophotometry for pigment orientation and concentration. Methods in Enzymology 81:642–647

    Google Scholar 

  • Hartwig HG (1975) Neurobiologische Studien an photoneuroendokrinen Systemen. Habil Thesis, Justus Liebig Univ. Gießen

    Google Scholar 

  • Hartwig HG (1982) Synchrone Erneuerung der Außengliedstrukturen in der Epiphysis cerebri bei Rana esculenta. 3. Arbeitstagung der Anat. Ges., Würzburg 6.–8. Okt. 1982, Anat Anz Suppl (im Druck)

  • Hartwig HG, Baumann C (1974) Evidence for photosensitive pigments in the pineal complex of the frog. Vision Res 14:597–598

    Google Scholar 

  • Hartwig HG, Oksche A (1982) Neurobiological aspects of extraretinal photoreceptive systems: structure and function. Experientia 38:991–996

    Google Scholar 

  • Hartwig HG, Pfautsch M (1973) Rasterelektronenmikroskopische Beobachtungen an pinealen Sinneszellen der Forelle, Salmo gairdneri (Teleostei). Z Zellforsch 138:585–589

    Google Scholar 

  • Hartwig HG, Van Veen Th (1979) Spectral characteristics of visible radiation penetrating into the brain and stimulating extraretinal photoreceptors. J Comp Physiol 130:277–282

    Google Scholar 

  • Heller J (1969) Comparative study of a membrane protein. Characterization of bovine, rat and frog visual pigments. Biochemistry 8:675–678

    Google Scholar 

  • Hill C (1894) The epiphysis of teleosts and Amia. J Morphol 9:237–268

    Google Scholar 

  • Joss JMP (1973) Pineal-gonad relationship in the lamprey Lampetra fluviatilis. Gen Comp Endocrinol 21:118–122

    Google Scholar 

  • Kavaliers M (1979) The pineal organ and circadian organization of teleost fish. Rev Can Biol 38:281–292

    Google Scholar 

  • Korf HW (1974) Acetylcholinesterase-positive neurons in the pineal and parapineal organs of the rainbow trout, Salmo gairdneri (With special reference to the pineal tract). Cell Tissue Res 155:475–489

    Google Scholar 

  • Korf HW, Wagner U (1981) Nervous connections of the parietal eye in adult Lacerta s. sicula Rafinesque as demonstrated by anterograde and retrograde transport of horseradish peroxidase. Cell Tissue Res 219:567–583

    Google Scholar 

  • Korf HW, Liesner R, Meissl H, Kirk A (1981) Pineal complex of the clawed toad, Xenopus laevis Daud.: Structure and function. Cell Tissue Res 216:113–130

    Google Scholar 

  • Korf HW, Zimmermann NH, Oksche A (1982) Intrinsic neurons and neural connections of the pineal organ of the house sparrow, Passer domesticus, as revealed by anterograde and retrograde transport of horseradish peroxidase. Cell Tissue Res 222:243–260

    Google Scholar 

  • La Motte I de (1963) Untersuchungen zur vergleichenden Physiologie der Lichtempfindlichkeit geblendeter Fische. Naturwissenschaften 50/9:363

    Google Scholar 

  • Liebman PA (1972) Microspectrophotometry of photoreceptors. In: Dartnall HJA (ed) The handbook of sensory physiology VII/1, Springer, Berlin Heidelberg New York, pp 481–528

    Google Scholar 

  • Loew ER, Dartnall HJA (1976) Vitamin A1/A2-based visual pigment mixtures in cone of the rudd. Vision Res 16:891–896

    Google Scholar 

  • Loew ER, Lythgoe JN (1978) The ecology of cone pigments in teleost fishes. Vision Res 18:715–722

    Google Scholar 

  • Matsuura T, Herwig HJ (1981) Histochemical and ultrastructural study of the nervous elements in the pineal organ of the eel, Anguilla anguilla. Cell Tissue Res 216:545–557

    Google Scholar 

  • Mayor HD, Hampton JC, Rosario B (1961) A simple method for removing the resin from epoxy-embedded tissue. J Biophys Biochem Cytol 9:909–910

    Article  CAS  PubMed  Google Scholar 

  • McNulty JA (1981) Synaptic ribbons in the pineal organ of the goldfish: circadian rhythmicity and the effect of constant light and constant darkness. Cell Tissue Res 215:491–497

    Google Scholar 

  • Meiniel A (1969) Cellules de type photorécepteur dans la rétine dorsale de l'organe parapinéal d'ammocète de Lampetra planeri. C R Acad Sci (Paris) Sér D 268:2265–2268

    Google Scholar 

  • Meiniel A (1971) Etude cytophysiologique de l'organe parapinéal de Lampetra planeri. J NeuroVisc Rel 32:157–199

    Google Scholar 

  • Meiniel A (1980) Ultrastructure of serotonin-containing cells in the pineal organ of Lampetra planeri (Petromyzontidae). A second sensory cell line from photoreceptor to pinealocyte. Cell Tissue Res 207:407–427

    Google Scholar 

  • Meiniel A (1981) New aspects of the phylogenetic evolution of sensory cell lines in the vertebrate pineal complex. Developments in Endocrinology 14:27–48

    Google Scholar 

  • Meiniel A, Collin JP (1971) Le complexe pinéal de l'ammocète (Lampetra planeri, Bl.). Identification de ganglion sous-jacent à l'organe parapinéal et relations épithalamique des organes pinéal et parapinéal. Z Zellforsch 117:354–380

    Google Scholar 

  • Meiniel A, Vivien-Roels B (1983) The presence of two populations of sensory-type cells in the pineal organ of the five-bearded rockling, Ciliata mustela L. (Pisces, Teleostei). Cell Tissue Res, in press

  • Meissl H, Dodt E (1981) Comparative physiology of pineal photoreceptor organs. Developments in Endocrinology 14:61–80

    Google Scholar 

  • Morita Y (1966) Entladungsmuster pinealer Neurone der Regenbogenforelle (Salmo irideus) bei Belichtung des Zwischenhirns. Pflügers Arch ges Physiol 289:155–167

    Google Scholar 

  • Morita Y (1975) Direct photosensory activity of the pineal. In: Knigge KM, Scott DE, Kobayashi H, Ishii S (eds) Brain-Endocrine-Interaction II. The ventricular system, Karger, Basel, pp 376–387

    Google Scholar 

  • Morita Y, Dodt E (1971) Photosensory responses from the pineal eye of the lamprey (Petromyzon fluviatilis). Proc Int Physiol Sci 25th, Munich 9:405

    Google Scholar 

  • Morita Y, Dodt E (1973) Slow photic responses of the isolated pineal organ of lamprey. Nova Acta Leopoldina 38:331–339

    Google Scholar 

  • Nilsson SEG, Crescitelli F (1970) A correlation of ultrastructure and function in the developing retina of the frog tadpole. J Ultrastruct Res 30:87–102

    Google Scholar 

  • Oksche A (1965) Survey of the development and comparative morphology of the pineal organ. Progr Brain Res 10:3–29

    Google Scholar 

  • Oksche A, Hartwig HG (1975) Photoneuroendocrine systems and the third ventricle. In: Knigge KM, Scott DE, Kobayashi H, Ishii S (eds) Brain-endocrine interaction II. The ventricular system, Karger, Basel, pp 40–53

    Google Scholar 

  • Oksche A, Hartwig HG (1979) Pineal sense organs — components of photoneuroendocrine systems. Progr Brain Res 52:113–130

    Google Scholar 

  • Oksche A, Vaupel-von Harnack M (1965) Vergleichende elektronenmikroskopische Studien am Pinealorgan. Progr Brain Res 10:237–258

    Google Scholar 

  • Omura Y (1979) Light and electron microscopic studies on the pineal tract of rainbow trout, Salmo gairdneri. Rev Can Biol 38:105–118

    Google Scholar 

  • Omura Y, Ali MA (1980) Responses of pineal photoreceptors in the brook and rainbow trout. Cell Tissue Res 208:111–122

    Google Scholar 

  • Papermaster DS, Converse CA, Siu J (1975) Membrane biosynthesis in the frog retina: opsin transport in the photoreceptor cell. Biochemistry 14:1343–1352

    Google Scholar 

  • Papermaster DS, Converse CA, Zorn MA (1976) Biosynthesis and immunocytochemical characterization of a large protein in frog and cattle rod outer segment membranes. Exp Eye Res 23:105–116

    Google Scholar 

  • Papermaster DS, Schneider BG, Zorn MA (1978) Immunocytochemical localization of opsin in outer segments and Golgi zones of frog photoreceptor cells. An electron microscope analysis of cross-linked albumin-embedded retinas. J Cell Biol 77:196–120

    Google Scholar 

  • Pu GA, Dowling JE (1981) Anatomical and physiological characteristics of pineal photoreceptor cell in the larval lamprey, Petromyzon marinus. J Neurophysiol 46:1018–1038

    Google Scholar 

  • Röhlich P (1976) Photoreceptor membrane carbohydrate on the intradiscal surface of retinal rod disks. Nature 263:789–791

    Google Scholar 

  • Rüdeberg C (1969) Structure of the parapineal organ of the adult rainbow trout, Salmo gairdneri Richardson. Z Zellforsch 93:282–304

    Google Scholar 

  • Rüdeberg C (1971) Structure of the pineal organ of Anguilla anguilla L. and Lebistes reticulatus Peters (Teleostei). Z Zellforsch 122:227–243

    Google Scholar 

  • Schwanzara SA (1967) The visual pigments of freshwater fishes. Vision Res 7:121–148

    Google Scholar 

  • Stell WK, Hárosi FI (1976) Cone structure and visual pigment content in the retina of the goldfish. Vision Res 16:647–658

    Google Scholar 

  • Studnička FK (1893) Sur les organes pariétaux de Petromyzon planeri. Sitzung Gesellschaft Wissenschaft (Prague): 1–50

  • Studnička FK (1905) Die Parietalorgane. In: Oppel A (ed) Lehrbuch der vergleichenden mikroskopischen Anatomie der Wirbeltiere. Vol 5 A, Fischer, Jena, pp 1–254

    Google Scholar 

  • Tabata M, Tamura T, Niwa H(1975) Origin of the slow potential in the pineal organ of the rainbow trout. Vision Res 15:737–740

    Google Scholar 

  • Tilney F, Warren LF (1919) The morphology and evolutional significance of the pineal body. Am Anat Memoirs 9:1–257

    Google Scholar 

  • Tretjakoff D (1915) Die Parietalorgane von Petromyzon fluviatilis. Z wiss Zool 113:1–112

    Google Scholar 

  • Tsin ATC, Liebman PA, Beatty DD, Drzymaka R (1981) Rod and cone visual pigment in the goldfish. Vision Res 21:943–946

    Google Scholar 

  • Ueck M (1979) Innervation of the vertebrate pineal. Progr Brain Res 52:45–88

    Google Scholar 

  • Ueck M (1981) Variation in structure and function of the pineal systems. Developments in Endocrinology 14:151–168

    Google Scholar 

  • Van Veen Th (1981) A study on the basis for zeitgeber entrainment. With special reference to extraretinal photoreception in the eel. Dr phil thesis, Mat Nat Fac Univ Lund

    Google Scholar 

  • Van Veen Th (1982) The pineal and parapineal organs of the elver (Anguilla anguilla L.). Cell Tissue Res 222:433–444

    Google Scholar 

  • Van Veen Th, Andersson H (1982) Threshold for synchronization of locomotor activity to visible radiation in the eel Anguilla anguilla. OIKOS 38:21–26

    Google Scholar 

  • Van Veen Th, Hartwig HG, Müller K (1976) Light-dependent motor activity and photonegative behavior in the eel (Anguilla anguilla L.). Evidence for extraretinal and extrapineal photoreception. J Comp Physiol 111:209–219

    Google Scholar 

  • Vigh B, Vigh-Teichmann I (1981) Light- and electron-microscopic demonstration of immunoreactive opsin in the pinealocytes of various vertebrates. Cell Tissue Res 221:451–463

    Google Scholar 

  • Vigh B, Vigh-Teichmann I, Aros B (1975) Comparative ultrastructure of cerebrospinal fluid-contacting neurons and pinealocytes. Cell Tissue Res 158:409–424

    Google Scholar 

  • Vigh B, Vigh-Teichmann I, Röhlich P, Aros B (1982) Immunoreactive opsin in the pineal organ of reptiles and birds. Z mikr-anat Forsch 96:113–129

    Google Scholar 

  • Vigh-Teichmann I (1981) The pineal eye of vertebrates. Acta Anat 111:155

    Google Scholar 

  • Vigh-Teichmann I, Röhlich P, Vigh B, Aros B (1980a) Comparison of the pineal complex, retina and cerebrospinal fluid-contacting neurons by immunocytochemical antirhodopsin reaction. Z mikr-anat Forsch 94:623–640

    Google Scholar 

  • Vigh-Teichmann I, Vigh B, Röhlich P, Olsson R (1980b) Phylogenetic aspects of the sensory neurons of the wall of the diencephalon. In: Spatz M, Mrsulja BB, Rakic LjM, Lust WD (eds) Circulatory and developmental aspects of brain metabolism, Plenum Press, New York, pp 415–428

    Google Scholar 

  • Vigh-Teichmann I, Korf HW, Oksche A, Vigh B (1982a) Opsin-immunoreactive outer segments and acetylcholinesterase positive neurons in the pineal complex of Phoxinus phoxinus (Teleostei, Cyprinidae). Cell Tissue Res 227:351–370

    Google Scholar 

  • Vigh-Teichmann I, Vigh B, Manzano e Silva MJ, Aros B (1983) The pineal organ of Raja clavata: Opsin immunoreactivity and ultrastructure. Cell Tissue Res 228:139–148

    Google Scholar 

  • Vigh-Teichmann I, Korf HW, Nürnberger F, Oksche A, Vigh B (1982b) Vergleichende immuncytochemische Studien an pinealen Photorezeptoren und Liquorkontaktneuronen. Verh Anat Ges 77, im Druck

  • Vivien-Roels B (1981) Pineal control of reproduction in non-mammalian vertebrates. Developments in Endocrinology 14:315–334

    Google Scholar 

  • Vollrath L (1981) The pineal organ. In: Oksche A, Vollrath L (eds) Handbuch der mikroskopischen Anatomie des Menschen VI/7, Springer, Berlin Heidelberg New York

    Google Scholar 

  • Yamada E (1982) Morphology of vertebrate photoreceptors. Methods in Enzymology 81:3–17

    Google Scholar 

  • Young JZ (1935) The photoreceptors of lampreys. II. The function of the pineal complex. J Exp Biol 12:254–270

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Cytobiology, Justus Liebig University, Giessen, Germany

    I. Vigh-Teichmann,  H. -W. Korf, F. Nürnberger, A. Oksche, B. Vigh & R. Olsson

  2. Second Department of Anatomy, Histology and Embryology, Semmelweis University, Medical School, Budapest, Hungary

    I. Vigh-Teichmann,  H. -W. Korf, F. Nürnberger, A. Oksche, B. Vigh & R. Olsson

  3. Zoological Institute, University of Stockholm, Stockholm, Sweden

    I. Vigh-Teichmann,  H. -W. Korf, F. Nürnberger, A. Oksche, B. Vigh & R. Olsson

Authors
  1. I. Vigh-Teichmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. -W. Korf
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. Nürnberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Oksche
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. Vigh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R. Olsson
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Dedicated to Professor E. Dodt, Max Planck Institute for Physiological and Clinical Research, Bad Nauheim, FRG, on the occasion of his 60th birthday

This investigation was supported by grants from the Deutsche Forschungsgemeinschaft to A.O. (Ok 1/25: Mechanismen biologischer Uhren) and to H.W.K. (Ko 758/1; 758/2-2), and from the Swedish Natural Research Sciences Council to R.O. (Nr. 2124)

On leave from the 2nd Department of Anatomy, Semmelweis OTE, Budapest, Hungary

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vigh-Teichmann, I., Korf, H.W., Nürnberger, F. et al. Opsin-immunoreactive outer segments in the pineal and parapineal organs of the lamprey (Lampetra fluviatilis), the eel (Anguilla anguilla), and the rainbow trout (Salmo gairdneri). Cell Tissue Res. 230, 289–307 (1983). https://doi.org/10.1007/BF00213806

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00213806

Key words

Search

Navigation